Concept: Commensalism

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The interactions between intestinal microbiota, immune system, and pathogens describe the human gut as a complex ecosystem, where all components play a relevant role in modulating each other and in the maintenance of homeostasis. The balance among the gut microbiota and the human body appear to be crucial for health maintenance. Intestinal parasites, both protozoans and helminths, interact with the microbial community modifying the balance between host and commensal microbiota. On the other hand, gut microbiota represents a relevant factor that may strongly interfere with the pathophysiology of the infections. In addition to the function that gut commensal microbiota may have in the processes that determine the survival and the outcome of many parasitic infections, including the production of nutritive macromolecules, also probiotics can play an important role in reducing the pathogenicity of many parasites. On these bases, there is a growing interest in explaining the rationale on the possible interactions between the microbiota, immune response, inflammatory processes, and intestinal parasites.

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An extensive body of evidence documents the importance of the gut microbiome both in health and in a variety of human diseases. Cell and animal studies describing this relationship abound, whilst clinical studies exploring the associations between changes in gut microbiota and the corresponding metabolites with neurodegeneration in the human brain have only begun to emerge more recently. Further, the findings of such studies are often difficult to translate into simple clinical applications that result in measurable health outcomes. The purpose of this paper is to appraise the literature on a select set of faecal biomarkers from a clinician’s perspective. This practical review aims to examine key physiological processes that influence both gastrointestinal, as well as brain health, and to discuss how tools such as the characterisation of commensal bacteria, the identification of potential opportunistic, pathogenic and parasitic organisms and the quantification of gut microbiome biomarkers and metabolites can help inform clinical decisions of nutrition and lifestyle medicine practitioners.

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Despite the accepted health benefits of consuming dietary fiber, little is known about the mechanisms by which fiber deprivation impacts the gut microbiota and alters disease risk. Using a gnotobiotic mouse model, in which animals were colonized with a synthetic human gut microbiota composed of fully sequenced commensal bacteria, we elucidated the functional interactions between dietary fiber, the gut microbiota, and the colonic mucus barrier, which serves as a primary defense against enteric pathogens. We show that during chronic or intermittent dietary fiber deficiency, the gut microbiota resorts to host-secreted mucus glycoproteins as a nutrient source, leading to erosion of the colonic mucus barrier. Dietary fiber deprivation, together with a fiber-deprived, mucus-eroding microbiota, promotes greater epithelial access and lethal colitis by the mucosal pathogen, Citrobacter rodentium. Our work reveals intricate pathways linking diet, the gut microbiome, and intestinal barrier dysfunction, which could be exploited to improve health using dietary therapeutics.

An incidental observation of the fly Philornis downsi parasitizing a Galapagos Flycatcher (Myiarchus magnirostris) nest has revealed new insights into the searching behavior and biology of this invasive fly parasite and its interactions with endemic land birds in the Galapagos Islands. Observations suggest that P. downsi relies on olfactory cues, or olfactory cues combined with the activity of adult birds, to locate nests and that flies continue to visit nests when chicks are >3 d old. At least 200 eggs were laid by P. downsi in different parts of the nest and >40 early-instar larvae were found inside the head of one chick, with additional larvae found in the base of the nest. Parasitism was the likely cause of mortality of both chicks found in or near the nest. This is the first published description of P. downsi parasitizing chicks of M. magnirostris and highlights the vulnerability of this endemic bird species to this invasive fly.

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Environmentally induced alterations in the commensal microbiota have been implicated in the increasing prevalence of food allergy. We show here that sensitization to a food allergen is increased in mice that have been treated with antibiotics or are devoid of a commensal microbiota. By selectively colonizing gnotobiotic mice, we demonstrate that the allergy-protective capacity is conferred by a Clostridia-containing microbiota. Microarray analysis of intestinal epithelial cells from gnotobiotic mice revealed a previously unidentified mechanism by which Clostridia regulate innate lymphoid cell function and intestinal epithelial permeability to protect against allergen sensitization. Our findings will inform the development of novel approaches to prevent or treat food allergy based on modulating the composition of the intestinal microbiota.

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Intestinal dwelling parasites have evolved closely with the complex intestinal microbiota of their host, but the significance of the host microbiota for metazoan pathogens and the role of their own intestinal microbiota are still not fully known. We have found that the parasitic nematodeTrichuris murisacquired a distinct intestinal microbiota from its host, which was required for nematode fitness. Infection of germ-free mice and mice monocolonized withBacteroides thetaiotaomicrondemonstrated that successfulT. murisinfections require a host microbiota. Following infection,T. muris-induced alterations in the host intestinal microbiota inhibited subsequent rounds of infection, controlling parasite numbers within the host intestine. This dual strategy could promote the long-term survival of the parasite within the intestinal niche necessary for successful chronic nematode infection.

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Climate change is a well-documented driver of both wildlife extinction and disease emergence, but the negative impacts of climate change on parasite diversity are undocumented. We compiled the most comprehensive spatially explicit data set available for parasites, projected range shifts in a changing climate, and estimated extinction rates for eight major parasite clades. On the basis of 53,133 occurrences capturing the geographic ranges of 457 parasite species, conservative model projections suggest that 5 to 10% of these species are committed to extinction by 2070 from climate-driven habitat loss alone. We find no evidence that parasites with zoonotic potential have a significantly higher potential to gain range in a changing climate, but we do find that ectoparasites (especially ticks) fare disproportionately worse than endoparasites. Accounting for host-driven coextinctions, models predict that up to 30% of parasitic worms are committed to extinction, driven by a combination of direct and indirect pressures. Despite high local extinction rates, parasite richness could still increase by an order of magnitude in some places, because species successfully tracking climate change invade temperate ecosystems and replace native species with unpredictable ecological consequences.

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Highly social ants, bees and wasps employ sophisticated recognition systems to identify colony members and deny foreign individuals access to their nest. For ants, cuticular hydrocarbons serve as the labels used to ascertain nest membership. Social parasites, however, are capable of breaking the recognition code so that they can thrive unopposed within the colonies of their hosts. Here we examine the influence of the socially parasitic slave-making ant, Polyergus breviceps on the nestmate recognition system of its slaves, Formica altipetens. We compared the chemical, genetic, and behavioral characteristics of colonies of enslaved and free-living F. altipetens. We found that enslaved Formica colonies were more genetically and chemically diverse than their free-living counterparts. These differences are likely caused by the hallmark of slave-making ant ecology: seasonal raids in which pupa are stolen from several adjacent host colonies. The different social environments of enslaved and free-living Formica appear to affect their recognition behaviors: enslaved Formica workers were less aggressive towards non-nestmates than were free-living Formica. Our findings indicate that parasitism by P. breviceps dramatically alters both the chemical and genetic context in which their kidnapped hosts develop, leading to changes in how they recognize nestmates.

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Birds are known to respond to nest-dwelling parasites by altering behaviours. Some bird species, for example, bring fresh plants to the nest, which contain volatile compounds that repel parasites. There is evidence that some birds living in cities incorporate cigarette butts into their nests, but the effect (if any) of this behaviour remains unclear. Butts from smoked cigarettes retain substantial amounts of nicotine and other compounds that may also act as arthropod repellents. We provide the first evidence that smoked cigarette butts may function as a parasite repellent in urban bird nests. The amount of cellulose acetate from butts in nests of two widely distributed urban birds was negatively associated with the number of nest-dwelling parasites. Moreover, when parasites were attracted to heat traps containing smoked or non-smoked cigarette butts, fewer parasites reached the former, presumably due to the presence of nicotine. Because urbanization changes the abundance and type of resources upon which birds depend, including nesting materials and plants involved in self-medication, our results are consistent with the view that urbanization imposes new challenges on birds that are dealt with using adaptations evolved elsewhere.

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There has been a dramatic rise in the prevalence of IgE-mediated food allergy over recent decades, particularly among infants and young children. The cause of this increase is unknown but one putative factor is a change in the composition, richness and balance of the microbiota that colonize the human gut during early infancy. The coevolution of the human gastrointestinal tract and commensal microbiota has resulted in a symbiotic relationship in which gut microbiota play a vital role in early life immune development and function, as well as maintenance of gut wall epithelial integrity. Since IgE mediated food allergy is associated with immune dysregulation and impaired gut epithelial integrity there is substantial interest in the potential link between gut microbiota and food allergy. Although the exact link between gut microbiota and food allergy is yet to be established in humans, recent experimental evidence suggests that specific patterns of gut microbiota colonization may influence the risk and manifestations of food allergy. An understanding of the relationship between gut microbiota and food allergy has the potential to inform both the prevention and treatment of food allergy. In this paper we review the theory and evidence linking gut microbiota and IgE-mediated food allergy in early life. We then consider the implications and challenges for future research, including the techniques of measuring and analyzing gut microbiota, and the types of studies required to advance knowledge in the field.